A sensory system for mating in octopus.

Sensory systems for mate recognition maintain species boundaries and influence diversification. Thus, uncovering how molecules and receptors evolve to mediate this critical function is essential to understanding biodiversity. Male octopuses use a specialized arm called the hectocotylus to identify females and navigate their internal organs to reach the oviduct and deliver sperm. Here, we discovered that the hectocotylus is a dual sensory and mating organ that uses contact-dependent chemosensation of progesterone, a conserved ovarian hormone. We identified chemotactile receptors for progesterone and resolved the structural basis for their evolution from ancestral neurotransmitter receptors and subsequent expansion and tuning across cephalopods. These findings reveal principles by which sensory innovations shape reproductive behavior and suggest mechanisms for how sensory evolution contributes to the diversification of life. Editor's summary: Male octopuses use a specialized arm called the hectocotylus to navigate inside of the female mantle and toward the ovary to deposit spermatophores for fertilization. The mechanisms determining the success of this strategy have remained unknown. Villar et al. have now demonstrated that progesterone produced in female ovaries activates hectocotylus neural activity and autonomous movement and stimulates male mating search behavior (see the Perspective by Di Cosmo). Sensory cells in the hectocotylus expressing the receptor CRT1 are responsible for sensing progesterone. These results describe the molecular basis of a previously unrecognized sensory organ for mating in octopus and shed light on how sensory innovation determines reproductive success. —Mattia Maroso [ABSTRACT FROM AUTHOR]